Entomology 3rd edition - C.Gillott - Chapter 24 docx

However, with rare exceptions,for example, the honey bee and silkmoth whose management is relatively simple and labor-intensive, until recently humans neither desired nor were able, beca

be realized that the ecological principles governing the interactions between insects andhumans are no different from those between insects and any other living species, eventhough humans with their modern technology can modify considerably the nature of theseinteractions.

Of an estimated 5–10 million species of insects, probably not more than a fraction of1% interact, directly or indirectly, with humans Perhaps some 10,000 constitute pests that,either alone or in conjunction with microorganisms, cause significant damage or death tohumans, agricultural or forest products, and manufactured goods Worldwide food and fiberlosses caused by pests (principally insects, plant pathogens, weeds, and birds) are generallyestimated at about 40%, of which 12% are attributable to insects and mites These figures donot include postharvest losses, estimated to be about 20%, and occur despite the application

of about 3 million tonnes of pesticide (worth more than US$31 billion, including aboutUS$9 billion of insecticide) (Pimentel, 2002) In the United States alone, crop losses related

to insect damage rose from 7% to 13% in the period 1945–1989, despite a tenfold increase

in the amount of insecticide used (>120,000 tonnes each year) (Pimentel et al., 1992).

On the other hand, the value of benefits derived from insects is severalfold that of losses

as a result of their pollinating activity, their role in biological control, and their importance ashoney, silk, and wax producers That insects do more good than harm probably would come

as a surprise to laypersons whose familiarity with insects is normally limited to mosquitoes,houseflies, cockroaches, various garden pests, etc., and to farmers who must protect theirlivestock and crops against a variety of pests If asked to prepare a list of useful insects, manypeople most likely would not get further than the honey bee and, perhaps, the silkmoth, andwould entirely overlook the enormous number of species that act as pollinating agents orprey on harmful insects that might otherwise reach pest proportions

Humans have long recognized the importance of insects in their well-being Insectsand/or their products have been eaten by humans for thousands of years Production of silkfrom silkmoth pupae has been carried out for almost 5000 years Locust swarms, which

725

CHAPTER 24

originally may have been an important seasonal food for humans, took on new significance ashumans turned to a farming rather than a hunting existence However, with rare exceptions,for example, the honey bee and silkmoth whose management is relatively simple and labor-intensive, until recently humans neither desired nor were able, because of a lack of basicknowledge as well as technology, to attempt large-scale modification of the environment

of insects, either to increase the number of beneficial insects or to decrease the number ofthose designated as pests

Several features of recent human evolution have made such attempts imperative Theseinclude a massive increase in population, a trend toward urbanization, increased geographicmovement of people and agricultural products, and, associated with the need to feed morepeople, a trend toward monoculture as an agricultural practice

The relatively crowded conditions of urban areas enable insects parasitic on humansboth to locate a host (frequently a prerequisite to reproduction) and to transfer between hostindividuals Thus, urbanization facilitates the spread of insect-borne human diseases such

as typhus, plague, and malaria whose spectacular effects on human population are welldocumented For example, in the sixth century A.D plague was responsible for the death

of about 50% of the population in the Roman Empire, and “Black Death” killed a similarproportion of England’s population in the mid-1300s (Southwood, 1977)

An increasing need to produce more and cheaper food led, through agricultural anization, to the practice of monoculture, the growing of a crop over the same large area ofland for many years consecutively However, two faults of monoculture are (1) the ecosys-tem is simplified and (2) as the crop plant is frequently graminaceous (a member of the grassfamily, including wheat, barley, oats, rice, and corn), the ecosystem is artificially maintained

mech-at an early stage of ecological succession By simplifying the ecosystem, humans encouragethe buildup of populations of the insects that compete with them for the food being grown.Further, as the competing insects are primary consumers, that is, near the start of the foodchain, they typically have a high reproductive rate and short generation time In other words,populations of such species have the potential to increase at a rapid rate

A massive increase in human geographic movements and a concomitant increase intrade led to the transplantation of a number of species, both plant and animal, into areaspreviously unoccupied by them Some of these were able to establish themselves and,

in the absence of normal regulators of population (especially predators and parasitoids),increased rapidly in number and became important pests Sometimes, as humans colonizednew areas, some of the cultivated plants that were introduced proved to be an excellent food

for species of insects endemic to these areas For example, the Colorado beetle, Leptinotarsa

decemlineata, was originally restricted to the southern Rocky Mountains and fed on wild

Solanaceae With the introduction of the potato by settlers, the beetle had an alternate, moreeasily accessible source of food, as a result of which both the abundance and distribution ofthe beetle increased and the species became an important pest Likewise, the apple maggot,

Rhagoletis pomonella, apparently fed on hawthorn until apples were introduced into the

eastern United States (Horn, 1976)

2 Beneficial Insects

Insects may benefit humans in various ways, both directly and indirectly The mostobvious of the beneficial species are those whose products are commercially valuable.Considerably more important, however, are the insects that pollinate crop plants Other

727 INSECTS AND HUMANS

beneficial insects are those that are used as food, for biological control of pest insects and

plants, in medicine and in research For some of these useful species, humans modify their

environment so as to increase their distribution and abundance in order to gain the benefits

2.1 Insects Whose Products Are Commercially Valuable

The best-known insects in this category are the honey bee (Apis mellifera(( ), silkworm

(Bombyx mori), lac insect (Laccifer lacca), and pela wax scale (Ericerus pela).

The honey bee originally occupied the African continent, most of Europe (except the

northern part), and western Asia, and within this area the usefulness of its products, honey

and beeswax, has been known for many thousands of years Though the discovery of sugar

in cane (in India, about 500 B.C.) and in beet (in Europe, about 1800 A.D.) (Southwood,

1977) led to a decline in the importance of honey, it is nevertheless still a very valuable

product

Bee management was probably first carried out by the ancient Egyptians Honey bees

were brought to North America by colonists in the early l600s, and today honey and

beeswax production is a billion dollar industry In 2001 world honey production was

esti-mated at about 1.25 million tonnes and a value of about US$4 billion China is the world’s

largest honey producer, accounting for almost 20% of the total; the United States lies in

third place (behind the former USSR), producing about 100,000 tonnes (with a value of

about US$330 million) (www.beekeeping.com/databases/honey-market/world honey.htm).

Beeswax is produced at the rate of about 1 kg for every 50–100 kg of honey; its value per

kilogram varies between one and three times that of honey There is a significant world

trade, perhaps worth about US$10 million annually, in pollen which is used not only by

beekeepers to supplement the reserves in the hive but also in the health-food industry

Other products that are collected include propolis (bee glue), venom (used to desensitize

patients with severe allergies to bee stings), and royal jelly which is added to certain food

supplements (Gochnauer, in Pimentel, 1991, Vol 2)

Good bee management aims to maintain a honey bee colony under optimum conditions

for maximum production Management details vary according to the climate and customs

of different geographical areas but may include (1) moving hives to locations where

nectar-producing plants are plentiful, (2) artificial feeding of newly established, spring colonies

with sugar syrup in order to build up colony size in time for the summer nectar flow,

(3) checking that the queen is laying well and, if not, replacing her, (4) checking and

treating colonies for diseases such as foulbrood and nosema, and (5) increasing the size of

a hive as the colony develops, in order to prevent swarming

Silk production has been commercially important for about 4700 years The industry

originated in East Asia and spread into Europe (France, Italy, and Spain) after eggs were

smuggled from China to Italy in the sixth century A.D The production of silk remains

a labor-intensive industry, making production costs high In 1988 world silk production

totaled about 67,000 tonnes, with raw silk fetching about US$50 per kilogram By the end

of 1998, production had increased slightly, to 72,000 tonnes, though the price of raw silk had

fallen to about US$26 per kilogram due to competition from cheaper synthetic fibers China

is the leading producer, with about 70% of the world total, and India has passed Japan as

the world’s second largest producer (Feltwell, 1990; www.tradeforum.org/news/fullstory).

The lac insect is a scale insect endemic to India and Southeast Asia that secretes about

itself a coating of lac, which may be more than 1 cm thick The twigs on which the insects

rest are collected and either used to spread the insects to new areas or ground up and heated

of wax some 5–10 mm thick Wax production peaked in the early 1900s and in a goodyear was more than 6000 tonnes Most of this wax was used in the manufacture of candles.Starting in the 1940s, with the coming of electricity and discovery of other waxes (notablyparaffin wax), interest in China wax production declined, and currently about 500 tonnes

is harvested yearly It is used for a variety of industrial, pharmaceutical, and horticulturalpurposes, for example, the manufacture of molds for precision instruments, insulation ofelectrical cables and equipment, production of high-gloss, tracing, and wax paper, as aningredient of furniture and automobile polishes, coating candies and pills, and as a graftingagent for fruit trees (Qin, in Ben-Dov and Hodgson, 1994)

2.2 Insects as Pollinators

As was noted in Chapter 23, Section 3.2, an intimate, mutualistic relationship hasevolved between many species of insects and plants, in which plants produce nectar andpollen for use by insects, while the latter provide a transport system to ensure effective cross-pollination Though some crop plants are wind-pollinated, for example, cereals, a largenumber, including fruits, vegetables, and field crops such as clovers, rape, and sunflower,require the service of insects In addition, ornamental flowers are almost all insect-pollinated.The best known, though by no means the only, important insect pollinator is the honeybee, and it is standard practice in many parts of the world for fruit, seed, and vegetableproducers either to set up their own beehives in their orchards and fields or to contract thisjob out to beekeepers For example, in California about 1.4 million hives are rented annually

to augment natural pollination of almonds (about 50% of the hives), alfalfa, melons, and

other fruits and vegetables (Pimentel et al., 1992) Under such conditions, the value of bees

as pollinators may be up to 140 times their value as honey producers Using this factor, it

is estimated that the increased value of crops attributable to honey bee pollination in the United States is about US$15 billion each year [see Robinson et al (1989) for a detailed

analysis] This estimate does not take into account the value of other, natural pollinators

of crops, nor obviously has a value been placed on the importance of all pollinators of

non-crop plants, which are vital to species diversity and as food for wildlife

2.3 Insects as Agents of Biological Control

It is only relatively recently that humans have gained an appreciation of the importance

of insects in the regulation of populations of potentially harmful species of insects andplants In many instances, this appreciation was gained only when, as a result of humanactivity, the natural regulators were absent, a situation that was rapidly exploited by thesespecies whose status was soon elevated to that of pest In the first three examples givenbelow (taken from DeBach and Rosen, 1991), none of the organisms is a pest in its country

of origin because of the occurrence there of various insect regulators The discovery ofthese regulators, followed by their successful culture and release in the area where the pestoccurs, constitutes biological control (Section 4.3)

729 INSECTS AND HUMANS

Among the best-known examples of an introduced plant pest are the prickly pear cacti

(Opuntia spp.) taken into Australia as ornamental plants by early settlers Once established,

the plants spread rapidly so that by 1925 some 60 million acres of land were infested,

mostly in Queensland and New South Wales Surveys in both North and South America,

where Opuntia spp are endemic, revealed about 150 species of cactus-eating insects, of

which about 50 were judged to have biological control potential and were subsequently

sent to Australia for culture and trials Larvae of one species, Cactoblastis cactorum, a

moth, brought from Argentina in January, 1925, proved to have the required qualities and

within 10 years had virtually destroyed the cacti (Figure 24.1) Perhaps the most remarkable

feature of this success story is that only 2750 Cactoblastis larvae were brought to Australia,

of which only 1070 became adults From these, however, more than 100,000 eggs were

produced, and in February–March of 1926 more than 2.2 million eggs were released in

the field! Additional releases, and redistribution of almost 400 million field-produced eggs

until the end of 1929, ensured the project’s success

The classical example of an insect pest brought under biological control is the

cottony-cushion scale, Icerya purchasi, which was introduced into California, probably from

Australia, in the l860s Within 20 years, the scale had virtually destroyed the recently

established, citrus-fruit industry in southern California As a result of correspondence

be-tween American and Australian entomologists and of a visit to Australia by an American

entomologist, Albert Koebele, two insect species were introduced into the United States

as biological control agents for the scale The first, in 1887, was Cryptochaetum iceryae,

a parasitic fly, about which little is heard, though DeBach and Rosen (1991) consider that

it had excellent potential for control of the scale had it alone been imported However, the

abilities of this species appear to have been largely ignored with the discovery by Koebele of

the vedalia beetle, Rodolia cardinalis, feeding on the scale In total, only 514 vedalia were

brought into the United States, between November 1888 and March 1889, to be cultured on

caged trees infested with scale By the end of July 1889, the vedalia had reproduced to such

an extent that one orchardist, on whose trees about 150 of the imported beetles had been

placed for culture, reported having distributed 63,000 of their descendants since June 1! By

1890, the scale was virtually wiped out Similar successes in controlling scale by means of

vedalia or Cryptochaetum have been reported from more than 60 countries (Hokkanen, in

Pimentel, 1991, Vol 2)

A third example of an introduced pest being brought under control by biological agents

is the winter moth, Operophtera brumata, which, though endemic to Europe and parts of

Asia, was accidentally introduced into Nova Scotia in the 1930s Its initial colonization was

slow, and it did not reach economically significant proportions until the early 1950s, and by

1962 it had spread to Prince Edward Island and New Brunswick The larvae of the winter

moth feed on the foliage of hardwoods such as oak and apple Though more than 60

para-sites of the winter moth are known in western Europe, only 6 of these were considered to be

potential control agents and introduced into eastern Canada between 1955 and 1960 Two

of these, Cyzenis albicans, a tachinid, and Agrypon flaveolatum, an ichneumonid, became

established, but between them they brought the moth under control by 1963 Embree (in

Huffaker, 1971) noted that the two parasites are both compatible and supplementary to

each other When the density of moth larvae is high, C albicans, which is attracted to,

and lays its eggs near, feeding damage caused by the larvae, is a more efficient parasite

than A flaveolatum However, once in the vicinity of damage, it does not specifically seek

out winter moth larvae Thus, at lower density, it wastes eggs on non-susceptible

defolia-tors such as caterpillars of the fall cankerworm, Alsophila pometaria Hence, at low host

CHAPTER 24

(B) and after (C) release of Cactoblastis [From D F Waterhouse, 1991, Insects and humans in Australia, in: The

Insects of Australia, 2nd ed., Vol 1 (CSIRO, ed.), Melbourne University Press By permission of the Division of

Entomology, CSIRO.]

731 INSECTS AND HUMANS

densities, A flaveolatum is more effective because it oviposits specifically on winter moth

larvae

The three examples described above indicate one method whereby the importance of

biological control can be demonstrated, namely, by introduction of potential pests into areas

where natural regulators are absent Another way of demonstrating the same phenomenon

is to destroy the natural regulators in the original habitat, which enables potential pests

to undergo a population explosion This has been achieved frequently through the use of

non-selective insecticides For example, the use of DDT against the codling moth, Cydia

pomonella, in the walnut orchards of California, led to outbreaks of native frosted scale,

Lecanium pruinosum, which was unaffected by DDT, whereas its main predator, an

en-cyrtid, Metaphycus californicus, suffered high mortality (Hagen et al., in Huffaker, 1971).

Another Lecanium scale, L coryli, introduced from Europe in the 1600s, is a potentially

serious pest of apple orchards in Nova Scotia but is normally regulated by various natural

parasitoids (especially the chalcidoids Blastothrix sericea and Coccophagus sp.) and

preda-tors (especially mirid bugs) Experimentally it was clearly demonstrated in the 1960s that

application of DDT destroyed a large proportion of the Blastothrix and mirid population,

and this was followed in the next two years by medium to heavy scale infestations Recovery

of the parasite and predators was rapid, however, and by the third year after spraying the

scale population density had been reduced to its original value (MacPhee and MacLellan,

in Huffaker, 1971)

2.4 Insects as Human Food

As noted in the previous chapter, insects play a key role in energy flow through the

ecosystem, principally as herbivores but also as predators or parasites, which may

them-selves be consumed by higher-level insectivorous vertebrates In turn, some of these

ver-tebrates, notably freshwater fish and game birds, are eaten by humans Moreover, in many

parts of the world, insects (including grasshoppers and locusts, beetle larvae, caterpillars,

brood of ants, wasps and bees, termites, cicadas, and various aquatic species) historically

played, and continue to have, an important part as a normal component of the human diet

(DeFoliart, 1992, 1999)

Aboriginal people of the Great Basin region in the southwestern United States

tra-ditionally spent much time and effort harvesting a variety of insects, principally crickets,

grasshoppers, shore flies (Ephydridae) (especially the pupae), caterpillars, and ants (adults

and pupae) though bees, wasps, stoneflies, aphids, lice, and beetles were also consumed on

an opportunistic basis Some of the insects were eaten raw though most were baked or roasted

prior to being consumed; further, large quantities, especially of grasshoppers and crickets,

were dried and ground to produce a flour that was stored for winter use (Sutton, 1988)

In parts of southeastern Australia the aboriginals would seasonally gorge themselves

on bogong moths (Agrotis infusa(( ) which estivate from December through February in vast

numbers in high-altitude caves and rocky outcrops in the Southern Tablelands (Figure 24.2)

Some tribes would make an annual trek over a considerable distance (up to 200 km) to take

advantage of this seasonal food source, returning each year to the same area (Flood, 1980)

In some African countries (including Botswana, South Africa, Zaire, and Zimbabwe)

there is a thriving trade in mopanie caterpillars (Gonimbrasia belina), and when these are

in season, beef sales may show a significant decline A similar preference for insects over

meat is shown by the Yupka people of Colombia and Venezuela (Ruddle, 1973) Insects

are also eaten in many Asian countries; indeed, giant water bugs (Lethocerus indicus) and

CHAPTER 24

B

pattern on a cave wall Aboriginals harvested the moths in vast numbers by dislodging them with sticks and collecting them in nets or bark dishes held beneath [A, photograph by J Green B, from D F Waterhouse, 1991,

Insects and humans in Australia, in: The Insects of Australia, 2nd ed., Vol 1 (CSIRO, ed.), Melbourne University

Press By permission of the Division of Entomology, CSIRO.]

733 INSECTS AND HUMANS

pupae of the silkmoth (Bombyx mori) are exported to Asian community food stores in

the United States from Thailand and South Korea, respectively Mexico also used to ship

food insects to the United States, namely ahuahutle (Mexican caviar—the eggs of various

aquatic Hemiptera) and maguey worms (caterpillars of Aegiale hesperiaris, found on agave).

Shipment of ahuahutle to North America no longer occurs because of lake pollution, though

it can still be found in many markets and restaurants in Mexico and is exported to Europe

as bird and fish food Maguey worms are commonly eaten in Mexico and are exported

as gourmet food to North America, France and Japan (DeFoliart, 1992, 1999) However,

tourists who visit Mexico are probably more familiar with another caterpillar, the red agave

worm (Comadia redtenbachi), seen in bottles of mezcal!

There has been some increase in interest in the potential of insects as food, including

discussion of the subject at international conferences However, most North Americans

and Europeans have not yet been educated to the delights of insects, despite the efforts of

authors such as Taylor and Carter (1976), DeFoliart (1992, 1999), and Berenbaum (1995) to

increase the popularity of insects as food The western world’s bias against eating insects has

two negative impacts First, it may be seen as a missed opportunity Compared to livestock,

insects are much more efficient at converting plant material into animal material with high

nutritional value With relatively little research, industrial-scale mass production of food

insects should be possible Second, as less-developed areas of the world become increasingly

westernized, their populations may be expected to eat fewer insects This could lead to

nutritional problems in areas where the economy is already marginal (DeFoliart, 1999)

2.5 Soil-Dwelling and Scavenging Insects

By their very habit the majority of soil-dwelling insects are ignored by humans Only

those that adversely affect our well-being, for example, termites, wireworms, and cutworms,

normally “merit” our attention When placed in perspective, however, it seems probable that

the damage done by such pests is greatly outweighed by the benefits that soil-dwelling insects

as a group confer The benefits include aeration, drainage, and turnover of soil as a result of

burrowing activity Many species carry animal and plant material underground for nesting,

feeding, and/or reproduction, which has been compared to ploughing in a cover crop

Many insects, including a large number of soil-dwelling species, are scavengers; that

is, they feed on decaying animal or plant tissues, including dung, and thus accelerate the

return of elements to food chains In addition, through their activity they may prevent use of

the decaying material by other, pest insects, for example, flies Perhaps of special interest

are the dung beetles (Scarabaeidae), most species of which bury pieces of fresh dung for

use as egg-laying sites (Figure 24.3) Generally, the beetles are sufficiently abundant that a

pat of fresh dung may completely disappear within a few hours, thus reducing the number

of dung-breeding flies that can locate it Furthermore, the chances of fly eggs or larvae

surviving within the dung are very low because the dung is ground into a fine paste as the

beetles or their larvae feed Likewise, the survival of the eggs of tapeworms, roundworms,

etc., present in the dung producer, is severely reduced by this activity

In Australia there are an estimated 22 million cattle and 162 million sheep that

collec-tively produce 54 million tonnes of dung (measured as dry weight) each year! The cattle

dung especially provides food and shelter for many insects, including the larvae of two

fly pests, the introduced buffalo fly (Haematobia irritans exigua) in northern Australia

and the native bush fly (Musca vetustissima) in southeastern and southwestern areas of the

country Further, because of the generally dry climate, the dung soon dries and may remain

CHAPTER 24

pad and then buried This southern African species was introduced into Australia in 1973; and (B) diagrammatic

section through nest of the Australian native dung beetle Onthophagus compositus, which colonizes the dung of

kangaroos, wallabies, and wombats [A, photograph by J Green By permission of the Division of Entomology, CSIRO B, from G F Bornemissza, 1971, A new variant of the paracopric nesting type in the Australian dung

beetle, Onthophagus compositus, Pedobiologia 11:1–10 By permission of Gustav Fischer Verlag.]

735 INSECTS AND HUMANS

unchanged for a considerable time so that the fiber and nutrients are unavailable to maintain

soil fertility and texture Rank herbage grows around each dung pat, and this is not normally

eaten by cattle Thus, at any time, dung pats render a significant proportion (estimated at

about 20%) of all pasture potentially unusable (Waterhouse, 1974) Although Australia has

more than 320 indigenous species of dung beetles, almost all of these use only the dung

of native marsupials, especially kangaroos, wallabies, and wombats, and, furthermore, are

restricted to forest and woodland habitats Only a few species of the native Onthophagus

have adapted to using cattle dung (Waterhouse and Sands, 2001)

In 1963, it was decided to initiate a program of biological control of dung, and in

1967, after extensive research, various species of tropical southern African dung beetles

were released in northern Australia These species had been carefully selected from regions

climatically similar to northern Australia and because they were known to be effective

processors of the dung of large native ruminants The results were spectacular, the beetles

rapidly multiplied and spread over wide distances, while simultaneously achieving complete

or partial disposal of dung for much of the year (Waterhouse, 1974) Over the next 15 years,

about 50 additional species of dung beetles, plus a few species of histerid beetles that prey

on fly eggs, larvae, and puparia, were imported not only from southern Africa but also

from southern Europe and Asia, each having features appropriate to a particular region of

Australia Of the 50-odd species released, 25 dung beetles and 3 histerids have established

breeding populations in the field, though numbers (and effectiveness of dung processing)

may be highly varied according to the species, locality, season, and weather conditions

(Waterhouse and Sands, 2001) All of the species established in northern regions are common

in all except the winter months, and through the summer almost complete dispersal of

dung occurs Further, there is some evidence that such intense activity results in a regional

suppression of buffalo fly numbers

In the cooler southeast and southwest of Australia the introduced species are most active

in the summer and autumn months when their dung dispersal may substantially reduce bush

fly abundance However, their activity is generally low in winter and spring, the latter being

the period in southwestern Australia when massive populations of bush flies develop (Doube

et al., 1991) Thus, in 1989, three spring-active species were imported from Spain; one of

these, Bubas bison, established itself quickly though populations of the other two species

took longer to increase because of their complex breeding behavior (Creagh, 1993)

In terms of dung disposal, the Australian dung beetle project has been a major success,

saving farmers the costs of harrowing, accelerating the release of nutrients into the soil,

and reducing the availability of fly breeding sites No comprehensive study of the impact of

the introduced beetles on the pest fly problem has been undertaken However, Waterhouse

and Sands (2001) provide examples to show that the beetles may significantly reduce fly

populations at a local level, especially when rainfall, which prolongs the beetles’ breeding

activity, is favorable A compounding factor in any attempt to estimate the beetles’ impact is

the ease with which the flies are carried on wind currents from regions where they have bred

successfully This tends to mask local effects of dung beetle activity on fly numbers In all

probability the dung beetle system will become but one component of an integrated program

for fly population management, with other strategies being used when fly populations peak

2.6 Other Benefits of Insects

Their relatively simple food and other requirements, short generation time, and high

fecundity enable many insects to be reared cheaply and easily under laboratory conditions

CHAPTER 24

and, consequently, make them valuable in teaching and research Even at the pre-collegelevel, these attributes, plus their remarkable diversity of form and habits, make insects an

important resource both in and outside the classroom (Matthews et al., 1997) The fruit fly,

Drosophila melonagaster with its array of mutants, is familiar to all who take an elementary

college genetics class, though it must also be appreciated that the insect continues to have animportant role in advanced genetic research Studies on other insects have provided us withmuch of our basic knowledge of animal and cell physiology, particularly in the areas of nu-trition, metabolism, endocrinology, and neuromuscular physiology Investigations into thepopulation dynamics of some pest insects, especially forest species, led to the formulation

of some important concepts in population ecology (Gillott, 1985)

With the development of microbial resistance to many antibiotics, there has been arevival in the use of maggot therapy, the use of fly larvae to clean wounds and promote

healing (Sherman et al., 2000) Maggot therapy has been used for centuries in some societies

and probably developed as a result of casual observations that the larvae of some causing flies had beneficial effects on infected wounds Myiasis, the infestation of animaltissues (living or dead) by maggots, appears to have evolved in some Dipteran families thatwere originally saprophagous, that is, bred in carrion Currently, it is mostly seen in threefamilies: Oestridae (all 150 species), Sarcophagidae, and Calliphoridae (about 80 species

myiasis-in total) (Chapter 9, Section 3) However, most of these species are unsuitable for use myiasis-inmaggot therapy because they feed on healthy tissue, are highly host-specific, and haveother disadvantages Of the 10 or so species of “medicinal maggots,” the most common are

larvae of the greenbottle fly, Lucilia sericata Curiously, in the United Kingdom, continental

Europe, and New Zealand, this fly is a major sheep pest, causing “strike,” which may be

fatal in heavy infestations (Sherman et al., 2000).

Many insects give us pleasure through their aesthetic value Because of their beauty,certain groups, especially butterflies, moths, and beetles, are sometimes collected as a hobby.Some are embedded in clear materials from which jewelry, paperweights, bookends, placemats, etc., are made Others are simply used as models on which paintings and jewelry arebased

3 Pest Insects

Since humans evolved, insects have fed on them, competed with them for food andother resources, and acted as vectors of microorganisms that cause diseases in them or inthe organisms that they value However, as was noted in the Introduction, the impact of suchinsects increased considerably as the human population grew and became more urbanized.Urbanization presented easy opportunities for the dissemination of insect parasites on hu-mans and the diseases they carry Large-scale and long-term cultivation of the same cropover an area facilitated rapid population increases in certain plant-feeding species and thespread of plant diseases Modern transportation, too, encourages the spread of pest insectsand insect-borne diseases Further, as described in Section 2.3, some of the attempts at pesteradication have backfired, resulting in even greater economic damage

3.1 Insects That Affect Humans Directly

A large number of insect species may be external, or temporary internal, parasites of

humans Some of these are specific to humans, for example, the body louse (Pediculus

humanus) and pubic louse (Phthirus pubis), but most have a varied number of alternate

737 INSECTS AND HUMANS

California The mosquito, Culex tarsalis, is the primary vector of the virus, and house finches and house sparrows the

primary amplifying hosts (hosts in which the virus multiplies) Secondary (less important) amplifying hosts include

other passerine birds, chickens, and pheasants Another transmission cycle involves blacktail jackrabbits, which

are sometimes bitten by C tarsalis, and Aedes melaniman Humans and horses, as well as ground squirrels, tree

squirrels, and some other wild mammals become infected but do not contribute significantly to virus amplification.

[From J L Hardy, 1987, The ecology of western equine encephalomyelitis virus in the Central Valley of California,

1945–1985, Am J Trop Med Hyg 37(Suppl.):18S–32S By permission of the American Society of Tropical

Medicine and Hygiene.]

hosts which compounds the problem of their eradication With rare exceptions, for example,

some myiasis-causing flies, insect parasites are not fatal to humans In large numbers, insect

parasites may generally weaken their hosts, making them more susceptible to the attacks

of disease-causing organisms Or the parasites, as a result of feeding, may cause irritation

or sores which may then become infected

But by far the greatest importance of insects that parasitize humans is their role as

vectors of pathogenic microorganisms (including various “worms”) some well-known

ex-amples of which are given in Table 24.1 The pathogen is picked up when a parasitic insect

feeds and may or may not go through specific stages of its life cycle in the insect Bacteria

and viruses are directly transmitted to new hosts, an insect serving as a mechanical vector,

whereas for protozoa, tapeworms and nematodes, an insect serves as an intermediate host

in which an essential part of the parasites’ life cycle occurs (Figure 24.4) In the latter

arrangement the insect is known as a biological vector

A pathogen may reside (and multiply) in alternate vertebrate hosts that are immune to

or only mildly infected by it For example, the bacterium Pasteurella pestis, which causes

bubonic plague (Black Death), is endemic in wild rodent populations However, in domestic

rats and humans, to which it is transmitted by certain fleas, it is highly pathogenic Similarly,

in South America, yellow fever virus, transmitted by mosquitoes, is found in monkeys

though these are immune to it Such alternate hosts are thus important reservoirs of disease

739 INSECTS AND HUMANS

A third category of insects that directly affect humans includes those that may bite

or sting when accidental contact is made with them, for example, bees, wasps, ants, somecaterpillars (with poisonous hairs on their dorsal surface), and blister beetles Normally, theeffect of the bite or sting is temporary and nothing more than skin irritation, swelling, orblister formation Bee stings, however, may cause anaphylaxis or death in some sensitiveindividuals

3.2 Pests of Domesticated Animals

A range of insect parasites may cause economically important levels of damage todomestic animals The majority of these parasites are external and include bloodsuckingflies (e.g., mosquitoes, horse flies, deer flies, black flies, and stable flies), biting and suckinglice, and fleas Other parasites are internal for part of their life history, for example, bot,warble, and screwworm flies, which as larvae live in the gut (horse bot), under the skin(warble and screwworm of cattle), or in head sinuses (sheep bot) Other examples are given

in the chapters that deal with the orders of insects In addition to insects, other arthropods are

also important livestock pests, especially various mites and ticks Kunz et al (in Pimentel,

1991, Vol 1) estimated that direct losses caused by insect and tick pests of livestock werealmost $3 billion each year in the United States Insecticide treatment is routine for somepests, and in the absence of treatment, losses caused by these pests (e.g., cattle grubs,

Hypoderma bovis and H lineatum) might be as much as ten times greater Indirect losses

such as poor breeding performance by bulls, reduced conception rate by cows, and laborcosts of treating livestock are not included in the above estimate

Generally the effect of such parasites is to cause a reduction in the health of the infectedanimal In turn, this results in a loss of quality and/or quantity of meat, wool, hide, milk, etc.,produced When severely infected by parasites, an animal may eventually die In addition totheir own direct effect on the host, some parasites are vectors of livestock diseases, examples

of which are included in Table 24.1

3.3 Pests of Cultivated Plants

Damage to crops and other cultivated plants by insects is enormous; in the UnitedStates alone losses in potential production are estimated at 13% and have a value of aboutUS$30 billion annually, despite the application of more than 100,000 tonnes of insecti-cide Remarkably, about three quarters of the insecticide used is applied to 5% of the totalagricultural land, especially that growing row crops such as cotton, corn, and soybean (Pi-

mentel et al., in Pimentel, 1991, Vol 1) Damage is caused either directly by insects as

they feed (by chewing or sucking) or oviposit, or by viral, bacterial, or fungal diseases,for which insects serve as vectors Especially important as “direct damagers” of plants areOrthoptera, Lepidoptera, Coleoptera, and Hemiptera (see the chapters that deal with theseorders for specific examples of such pests) Several hundred diseases of plants are known to

be transmitted by insects (for examples see Table 24.2) including about 300 that are caused

by viruses (Eastop, 1977) Especially important in disease transmission are Hemiptera,

741 INSECTS AND HUMANS

Disease Important hosts Vectors Distribution

Viruses Alfalfa mosaic Alfalfa, tobacco, potato,

beans, peas, celery, zinnia, petunia

Aphids (at least 16 spp.)

incl Acyrthosiphon

primulae, A solani, Aphis craccivora, A fabae, A.

gossypii, Macrosiphum euphorbiae, M pisi, Myzus ornatus, M persicae, M.

maidis

North America, Australia, Denmark, Holland, UK

Bean common

mosaic

Beans Aphids (at least 11 spp.)

esp Aphis rumicis,

Macrosiphum pisi, M gei

mosaic

Cauliflower, cabbage, Chinese cabbage

Aphids esp Brevicoryne

brassicae, Rhopalosiphum pseudobrassicae, Myzus persicae

Europe, USA, New Zealand

Dahlia mosaic Dahlia, zinnia,

calendula

Aphids esp Myzus

persicae, Aphis fabae, A.

gossypii, Macrosiphum gei, Myzus convolvuli

Wherever dahlias are grown

Lettuce

mosaic

Lettuce, sweet pea, garden pea, endive, aster, zinnia

Aphids esp Myzus

persicae, Aphis gossypii, Macrosiphum euphorbiae

Europe, USA (esp.

California), New Zealand Pea mosaic Garden pea, sweet pea,

broadbean, lupin, clovers

Aphids: Acyrthosiphon

pisum, Myzus persicae, Aphis fabae, A rumicis

Europe, USA, New Zealand, Australia, Japan Potato virus Y Potato, tobacco, tomato,

petunia, dahlia

Aphids esp Myzus

persicae, M certus, M.

ornatus, Macrosiphum euphorbiae

UK, France, USA

Soybean

mosaic

Soybean Aphids incl Myzus

persicae, Macrosiphum pisi

Wherever soybean is grown

Sugarcane

mosaic

Sugarcane, com, sorghum, other tame and wild grasses

Numerous aphids incl.

Rhopalosiphum maidis, Aphis gossypii, Schizaphis graminum, Myzus persicae

Thrips: Thrips tabaci,

Frankliniella schultzeri, F rr fusca, F occidentalis

Africa, Asia, Australia, Europe, North and South America

(Continued)

Turnip, cauliflower, Chinese cabbage, kohlrabi, cabbage, Broccoli

Flea beetles (Phyllotreta

spp.); Mustard beetle

(Phaedon cochleariae);

Grasshoppers (Leptophyes

punctatissima, Chorthippus bicolor); Earwig (Forficula auricularia)

UK, Germany, Portugal, North America

Mycoplasmas Aster yellows Aster, celery, carrot,

squash, cucumber, wheat, barley

Numerous leafhoppers incl.

Gyponana hasta, Scaphytopius acutus, S.

irroratus, Macrosteles quadrilineatus, Paraphlepsius apertinus, rr Texananus ee (several species)

Worldwide

Clover phyllody

Most clovers Leafhoppers incl Aphrodes

albifrons, Macrosteles cristata M quadrilineatus,

M viridigriseus Euscelis lineolatus, E plebeja

Potato blackleg

Potato Seedcorn maggot (Hylemya

cilicrura), H trichodactyla

North America

Fire blight 90 spp of orchard trees

and ornamentals, esp.

apple, pear, quince

Wide range of insect vectors, esp bees, wasps, flies, Ants, aphids

North America, Europe

Fungi Dutch elm

disease

Elm Elm bark beetles, esp.

Scolytus multistriatus,

S scolytus, Hylurgopinus rufipes

Asia, Europe, North America

Ergot Cereals and other

grasses

About 40 spp of insects Esp.flies, beetles, aphids

Worldwide

aData from various sources.

particularly leafhoppers and aphids Three aspects of the behavior of these insects facilitatetheir role as disease vectors: (1) they make brief but frequent probes with their mouthpartsinto host plants; (2) as the population density reaches a critical level, winged migratoryindividuals are produced; and (3) in many species, winged females deposit a few progeny

on each of many plants, from which new colonies develop On the basis of their method

of transmission and viability (persistence in the vector), viruses may be arranged in three

743 INSECTS AND HUMANS

categories The non-persistent (stylet-borne) viruses are those believed to be transmitted

as contaminants of the mouthparts Such viruses remain infective in a vector for only a

very short time, usually an hour or less Semipersistent viruses are carried in the

ante-rior regions of the gut of a vector, where they may multiply to a certain extent Vectors

do not normally remain infective after a molt, presumably because the viruses are lost

when the foregut intima is shed Persistent (circulative or circulative-propagative) viruses

are those that, when acquired by a vector, pass through the midgut wall to the salivary

glands from where they can infect new hosts Such viruses may multiply within tissues of

a vector, which retains the ability to transmit the virus for a considerable time, in some

instances for the rest of its life Persistent viruses, in contrast to those in the first two

cate-gories, may be quite specific with respect to the vectors capable of transmitting them (Hull,

2002)

3.4 Insect Pests of Stored Products

Almost any stored material, whether of plant or animal origin, may be subject to attack

by insects, especially species of Coleoptera (larvae and adults) and Lepidoptera (larvae

only) Among the products that are frequently damaged are grains and their derivatives,

beans, peas, nuts, fruit, meat, dairy products, leather, and woolen goods In addition, wood

and its products may be spoiled by termites or ants Again, readers should refer to the

appropriate chapters describing these groups for specific examples

Estimates of the worldwide postharvest losses of foodstuffs (especially stored grains)

may be as high as 20%, of which about one-half is attributable to insects and the rest to

microorganisms, rodents, and birds Even in well-developed countries such as the United

States, Canada, and Australia where storage conditions are more adequate and pesticide

treatment is available, losses of 5% to 10% are estimated for stored grains Given a

world-wide estimate for the production of wheat, coarse grains, and rice as about 1.5 billion

tonnes in 1981–1982, perhaps as much as 150 million tons may have been lost as a

re-sult of insect damage The nature of the damage caused by stored products pests varies

Grain and other seed pests not only eat economically valuable quantities of food, but cause

spoilage by contamination with feces, odors, webbing, corpses, and shed skins, and by

creating heat and moisture damage that permits the growth of microorganisms (Wilbur

and Mills, in Pfadt, 1985) Pests of household goods such as clothing and furniture

prin-cipally cause damage by spoilage, for example, by tunneling, defecating, and creating

odors

4 Pest Control

As will be apparent from what was said above, pests are organisms that damage, to an

economically significant extent, humans or their possessions, or that in some other way are

a source of annoyance to humans Implicit in the above description are value judgments that

may vary according to who is making them, as well as where and when they are being made

Nevertheless, in a given set of circumstances, there will be an economic injury (annoyance)

threshold, measured in terms of a species’ population density, above which it is desirable

(profitable) to take control measures that will reduce the species’ density As the margin

between economic injury threshold and actual population density widens, the desirability

CHAPTER 24

TABLE 24.3 Principal Control Methods in Relation to Ecological Strategies of Pests

Control method: Pesticides

Biological control

Cultural control Genetic control

Examples (with Schistocerca gregaria (Most deciduous forest Oryctes rhinoceros

important (desert locust) pests, fruit pests, and (rhinoceros beetle) features): Fecundity/X = 400 eggs some vegetable pests) Fecundity/X = 50 eggs

Generation time = Generation time = 3–4

Migratory, defoliates Feeds on apical growing

(black bean aphid) (tsetse fly) Fecundity/X = 100 eggs Fecundity/X = 10 eggs Generation time = Generation time = 2–3

Feeds on wide range Feeds on narrow range of

Fecundity/X = 500 eggs Fecundity/X = 40 eggs Generation time = Generation time = 2–6

Feeds on organic Larvae feed on apple and

Fecundity/X = 1500 eggs Fecundity/X = 15 eggs Generation time = 1–1.5 Generation time = 1–2

Feeds on seedlings of External parasite of sheep most crops

a Data from Conway (1976) and Southwood (1977).

(profitability) of control increases Pest control is, then, essentially a sociological problem—

a matter of economics, politics, and psychology

A range of methods is available for the control of insect pests Each of these methodshas its advantages and disadvantages and these must be balanced against each other indetermining which (combination of) method(s) is most appropriate in a given instance.Some of these methods are spectacular but short-term and will be appropriate, for example,where massive outbreaks of pests are relatively sudden, yet unpredictable and temporary.Others are more slowly acting but relatively permanent in effect, and may be used for peststhat are more or less permanent but whose populations are relatively stable

Conway (1976) and Southwood (1977) proposed that pests can be arranged in a trum according to their “ecological strategies” and that the principal (best) method of control

spec-is based on their position in the spectrum (Table 24.3) At either end of the spectrum are

the so-called “r pests” and “K pests,” with the “intermediate pests” in between.

745 INSECTS AND HUMANS

The r pests are characterized by their potentially high rates of population increase

(resulting from the high fecundity and short generation time), well-developed powers of

dispersal (migration) and ability to locate new food sources, and rather general food

pref-erences These features enable r pests to colonize temporarily suitable habitats, in which

there is typically little interspecific competition for the resources available Because r pests

may occur in such large but unpredictable numbers and rapidly change their location,

preda-tors (of which there may be many) have relatively little effect on their population Further,

although like other organisms r pests are subject to disease, the latter is slow to take

ef-fect, by which time significant damage may have been done Finally, because of their high

reproductive potential, r pests are able to tolerate mass mortality and rapidly regenerate

their original density Hence, biological control, which is a relatively slow but long-term

method, is of little use against r pests For such pests specific insecticides, which can be

stored for application at short notice, continue to be the most important tool in their control

Included in the r -pest group are the “classic” pests: locusts, aphids, mosquitoes, and house

flies (Table 24.3)

K pests, on the other hand, have lower fecundity and longer generation time, poor

ability to disperse, relatively specialized food preferences, and are found in habitats that

re-main stable over long periods of time Under natural conditions, insects with the features of

K strategists seldom become pests If, however, probably as a result of human activity, their

niche is expanded (e.g., their food plant becomes an important crop), or if they can occupy

a new niche (e.g., feeding on domestic cattle rather than wild ungulates) they may become

a pest Once established, such pests are often difficult to eradicate over the short term,

for example, through the use of insecticides Insecticides are frequently not feasible tools

because the K pests attack the fruit rather than the foliage of crop plants, or because the cost

is prohibitive in view of the low density of the pest population (In some instances, however,

where even at low population density a pest may cause considerable damage, for example,

codling moth on apple, insecticidal control may be profitable.) Nor is biological control an

appropriate method because K pests have few natural enemies, a feature probably related

to their low density under natural conditions For K pests, the best methods of control are

those that disturb their habitat, for example, the breeding of resistant strains of plant(s) or

animal(s) attacked by the pests, and cultural practices Examples of K pests are given in

Table 24.3

The majority of pests are classified as intermediate pests in the Conway scheme because

they exhibit a mixture of the features of r and K pests For some of these, with a relatively

high reproductive potential, insecticidal control may be necessary under certain conditions,

and conversely, for pests approaching the K end of the spectrum, cultural control sometimes

may be adequate However, the most important feature of intermediate pests is the relatively

large number of natural enemies that they have These enemies, under normal circumstances,

are important regulators of the pest population In addition, intermediate pests are frequently

foliage- or root-damaging pests, for example, spruce budworm and some scale insects, and,

therefore, the economic injury threshold is reasonably high; that is, a fair amount of damage

can be tolerated without economic loss Hence, for these pests, biological control would

appear to be the single most appropriate method of control, which can be supplemented as

necessary with insecticidal and other methods The latter is, in other words, an integrated

control program

With these general considerations in mind, it is now appropriate to consider in more

detail the methods available for pest control

CHAPTER 24

4.1 Legal Control

Also known as regulatory control, legal control is based primarily on the old adage

“Prevention is better [in this instance, cheaper] than cure.” Legal control is the enactment

of legislation to prevent or control damage by insects (Rohwer, in Pimentel, 1991, Vol 1)

It includes, therefore, establishment of quarantine stations at major ports of entry into anarea Usually the stations are located at international borders, though in some instancesdomestic quarantines are necessary, for example, when certain parts of a country are widelyseparated from the rest (Hawaii and continental United States) At quarantine stations peo-ple and goods are inspected to prevent the accidental introduction of potential insect pestsand plant and animal diseases Prior to the introduction of quarantine legislation in theUnited States in the early 1900s (Plant Quarantine Act of 1912) a number of insect specieshad been accidentally introduced and become established as plant pests, for example, thecottony-cushion scale discussed in Section 2.3 Though quarantine has severely reducedthe number of insect introductions, on average 11 exotic species are still added annually

to the insect fauna of the United States (for a total of more than 800 for the period 1920–1980) About 35% of the important pests in the United States are introduced species and

include pink bollworm (Pectinophora gossypiella), citrus blackfly (Aleurocanthus wog-((

lumi), Egyptian alfalfa weevil (Hypera brunneipennis), face fly (Musca autumnalis), cereal

leaf beetle (Oulema melanopus), and Russian wheat aphid (Diuraphis noxia) (Sailer, 1983).

As an adjunct to quarantine, many countries (or areas within countries) have legislation thatrequires international or interstate shipments of animals or plants, or their products, to becertified as disease- or insect-free by qualified personnel prior to shipment

Also part of legal control is the setting up of surveillance systems for monitoring theinsect population in a given area so that, should an outbreak occur, it can be dealt withbefore it has a chance to spread Such surveillance is an important duty of state/provincialentomologists, in cooperation with local agriculture representatives and crop and livestockproducers

Another aspect of legal control, and one that has become increasingly important, isthe licensing of insecticides and the establishment of (1) regulations regarding their useand (2) monitoring systems to assess their total impact on the environment For example,

in the United States the Environmental Protection Agency is responsible for assessing theeffectiveness of pesticides, as well as their possible hazardous effects on humans, wildlife,and other organisms, including bees, other pollinating species, and beneficial parasitoids Asnoted earlier (Section 2.3), indiscriminate use of insecticides can result in greatly increasedrather than decreased pest damage

Until about 1940, insecticides belonged to two major categories, the “inorganics” andthe “botanicals.” Among the inorganic insecticides are arsenic and its derivatives (arseni-cals), including Paris green (copper acetoarsenite), which was the first insecticide to beused on a large scale in the United States—against Colorado potato beetle in 1865 Other

747 INSECTS AND HUMANS

inorganics include fluoride salts (developed at about the end of the 19th century,

follow-ing the realization that toxic residues were left by arsenicals), sulfur, borax, phosphorus,

mercury salts, and tartar These inorganic insecticides were typically sprayed on the pest’s

food plant or mixed with suitable bait In other words, all are “stomach poisons” that

re-quire ingestion and absorption to be effective Thus, they were unsatisfactory pesticides for

sucking insects for which “contact poisons,” absorbed through the integument or tracheal

system, are necessary

The “botanicals” are organic contact poisons produced by certain plants in which they

serve as protectants against insects (Chapter 23, Section 3.1) Among the earliest to be used

were (1) nicotine alkaloids, derived from certain species of Nicotiana, including N tabaca

(tobacco) (family Solanaceae); (2) rotenoids extracted from the roots of derris (Derris

spp.) and cub´e (´ Lonchocarpus spp.); and (3) pyrethroids, produced by plants in the genus

Because of their high mammalian toxicity, nicotine has been completely superseded

by synthetics, while rotenone use is now mainly restricted to control of some sucking pests

on crops and pests of pets and livestock The pyrethroids, when first available

commer-cially, were an important group of insecticides for use in the home, as livestock sprays,

and against stored-product, vegetable, or fruit pests, primarily because of their low toxicity

to mammals Initially, a major disadvantage of pyrethroids was their photolabile nature

(instability in light) and the need, therefore, to reapply them frequently made them

ex-pensive to use Thus, they were largely replaced by cheaper, synthetic insecticides in the

1940s, an important consequence of which was that relatively few insects became resistant

to them This feature, in conjunction with the development of several photostable

syn-thetic pyrethroids (e.g., cypermethrin, permethrin, fenvalerate, and deltamethrin), has led

to a resurgence in the importance of these compounds which now account for about one

third of world insecticide use (Elliott et al., 1978; Leahy, 1985; Pickett, 1988)

Unfor-tunately, but not surprisingly, paralleling this increased usage has been a major increase

in arthropod resistance to pyrethroids, from fewer than 10 species in 1970 to over 80 in

2003 (Metcalf, 1989; Georghiou and Lagunes-Tejeda, 1991; Resistant Arthropod Database,

2004)

Though two synthetic organic insecticides had been commercially available prior to

1939 (dinitrophenols in Germany, first used in 1892; organic thiocyanates in the United

States from 1932 on), it is generally acknowledged that this is the year in which the synthetic

organic insecticide industry took off After several years of research for a better

mothproof-ing compound, M¨uller, who worked for Geigy AG in Switzerland, discovered the value of

DDT as an insecticide In the next few years, production of DDT began at the company’s

plants in the United Kingdom and United States, although because of the Second World

War, knowledge of DDT was kept a closely guarded secret In early 1944, DDT was first

used on a large scale, in a delousing program in Naples where typhus had recently broken

out Some 1.3 million civilians were treated with DDT, and within 3 weeks the epidemic

was controlled (Fronk, in Pfadt, 1985) Later that year the identity of the “miracle cure”

was revealed, and the world soon became convinced that with DDT (and other recently

developed insecticides) pest insects would become a thing of the past In 1948 M¨uller was

awarded a Nobel Prize, though, interestingly, the first example of insect resistance to DDT

had been reported 2 years earlier!

Through the 1940s and into the 1960s, much research was carried out in Western Europe

and the United States for other insecticides as effective as DDT Initially, the search focused

on other chlorinated hydrocarbons, including lindane, chlordane, aldrin, dieldrin, endrin,

CHAPTER 24

and heptachlor, and more than 8 billion pounds were produced between 1950 and 1990(Casida and Quistad, 1998) The use of chlorinated hydrocarbons in the western worldwas severely reduced, beginning in the 1970s, following the development of resistanceand the recognition of the health hazards that these highly persistent insecticides pose (seebelow) Some, however, remain the major insecticides in some developing countries Thoughdiscovered in 1937, organophosphates such as TEPP, diazinon, dichlorvos, parathion, andmalathion did not come to prominence as insecticides till the mid-1960s They continue toplay a massive role, especially in agricultural pest control, with about one half of the top 20sales list being organophosphates (Casida and Quistad, 1998) Carbamates, for example,sevin, isolan, and furadan, originated in the 1940s but their impact on the insecticide scenewas not seen until the late 1960s They remain important with 4 representatives in the top

20 insecticides sold For details of structure, physical properties, formulation, lethal doses,usage, etc., consult Fronk, in Pfadt (1985), Volume 12 of Kerkut and Gilbert (1985), Hassall(1990), and Szmedra, in Pimentel (1991), Vol 1

The search for suitable synthetic insecticides continues today, though at a somewhatreduced rate because the profitability of such ventures for industrial concerns has greatlydiminished, for a variety of interrelated reasons The primary reasons are (1) the time andcost of discovery, development, and registration of an insecticide, estimated at an average

of 7 years and US$35–45 million, with an additional US$55–65 million for the cost of aproduction plant [by comparison, the total cost of developing a new drug is US$360 million(Casida and Quistad, 1998)] Only 1 in 15,000–20,000 candidate chemicals ever reachesthe marketing stage; (2) the relatively short “life expectancy” of an insecticide because ofthe development of resistance by its target organisms and/or its becoming an environmentalhazard In contrast to the situation 20–25 years ago, companies now seek to maximize saleswithin 3–5 years after registration; and (3) a general unwillingness of government agencies

to grant registrations for use of new insecticides (and, for that matter, other types of chemicalpesticides), as a result of pressure from environmentalists, special interest groups, and thegeneral public As a result, some of the largest companies in the chemical industry haveeither considerably reduced or abandoned research into the development of new insecticides(Brown, 1977; DeBach and Rosen, 1991; Dent, 2000)

Paralleling research into new synthetic insecticides has been the discovery of severaladditional groups of naturally occurring compounds with insecticidal activity, for example,the avermectins, spinosyns, and azadirachtins Avermectins, a mixture of natural products

from the soil actinomycete Streptomyces avermitilis, were discovered in the 1970s during

screening tests for natural antihelminthic compounds (Lasota and Dybas, 1991) It was alsoobserved that they were potent insecticides and acaricides, and subsequently ivermectinand abamectin were registered for use with domestic animals and some household pests.Ivermectin is also used to control onchocerciasis in West Africa and Latin America Thoughavermectins are quickly degraded in ultraviolet light and are strongly bound to soil particles,two features that improve their safety against non-target organisms, there are situations

in which they may pose problems For example, a large proportion of the avermectinsadministered to livestock pass unchanged out of the body in the feces These residuesremain in the dung pat for several weeks, to exert their toxic effects on a spectrum ofdung-using insects, both harmful (e.g., various flies) and beneficial (e.g., dung beetles).The situation is particularly of concern in Australia where, as noted in Section 2.5, a range

of exotic dung-beetle species have been introduced to deal with the massive amounts ofdung produced by domestic cattle and sheep Avermectins have been shown to exert a largenumber of detrimental effects on growth and reproduction of these beetles, though these

749 INSECTS AND HUMANS

effects can be significantly lessened by careful selection of the times when livestock are

treated (i.e., when the dung beetles are less active) However, the adoption of a

sustained-release bolus for delivery of the avermectins in livestock may have a major influence on

dung-beetle populations (Strong, 1992; Herd et al., 1993).

Spinosyns, discovered in the late 1980s, are produced by another actinomycete,

Sac-charopolyspora spinosa Like avermectins, spinosyns are easily degraded by ultraviolet

light and soil microorganisms They have low toxicity to mammals, birds, and non-target

(beneficial) insects Commercial preparations are available for control of a range of pests

on cotton, vegetables, turf, and ornamentals (Crouse and Sparks, 1998)

Azadirachtin is the major component of the oil extractable from the seeds and leaves

of the neem (margosa) tree (Azadirachta indica(( ), an evergreen endemic to southern and

southeastern Asia, but now found also in Africa, the United States, and Australia It has

been shown to exert a variety of potentially useful effects including inhibition of settling,

oviposition, and feeding behaviors, interference with both embryonic and postembryonic

development, reduction in number of eggs matured, and mortality, and it is effective on a

wide range of pest insects, especially phytophagous species Because azadirachtin is

pri-marily a feeding poison for juvenile phytophagous insects, it shows great selectivity in the

sense that the pests’ natural enemies (adult parasitoids and predators) are unaffected by it It

is also relatively non-toxic to vertebrates Offsetting these advantages are its limited

persis-tence in the field, its slow-acting nature, and, of course, the potential for the development of

resistance Nevertheless, it may become a useful adjunct to already available pesticides in

underdeveloped countries, and a few commercial preparations are available (Schmutterer,

1990; Isman et al., 1991; Gahukar, 1995; Beckage, in Rechcigl and Rechcigl, 2000).

Three major problems have arisen as a result of the massive use of insecticides over

the past 70 years First, many insects and mites have developed resistance to one or more

of the chemicals (Tables 24.4 and 24.5) (See Chapter 16, Section 5.5 for a discussion

TABLE 24.4 Number of Species of Insects and

Mites in Which Resistance to One or More Chemicals Has Been Documenteda

CHAPTER 24

TABLE 24.5 Number of Species of Arthropods with Reported Cases of Resistance

Through 2003a

Pesticide Groupb Importancec

DDT Cyclod OCL OP Carb Pyr Fum Other Med./Vet Agr Benef Other Total

aFrom Resistant Arthropod Database (2004)

bCyclod., cyclodiene; OCL, other chlorohydrocarbons; OP, organophosphate; Carb., carbamate; Pyr., pyrethroid; Fum., fumigant.

cMedVet., medical and veterinary pests; Agr., agricultural pests; Benef., predators, parasitoids, honey producers, etc.

of the mechanism of resistance.) Quadraspidiotus perniciosus (San Jose scale) is credited

with being the first recorded species to develop resistance to an insecticide (lime sulfur)

in 1908, less than 30 years after use of the insecticide began The house fly was the firstspecies resistant to a synthetic insecticide (DDT in 1946), and by 1989 the number of speciesshowing some resistance had reached more than 500, just over half of which are agriculturalpests Interestingly, between 1989 and 2003 the number of resistant species increased byonly 32 (Resistant Arthropod Database, 2004) Several reasons may be suggested for thisslow down in the appearance of resistant species: (1) Better use of insecticides as a result ofboth integrated pest management and resistance management; (2) highly diverse chemistry(and hence distinct modes of action) of currently used insecticides; (3) reduced fundingfor (hence less study of) resistance research; and (4) some degree of resistance has alreadydeveloped in most of the world’s worst arthropod pests (which number about 550 species)(Mark E Whalon, pers comm.)

Depending on the method of resistance developed by a species against an insecticide,species frequently have resistance to other chemicals of the same group (class resistance)

or even to chemicals of other groups (cross resistance) For example, the green peach aphid

(Myzus persicae) is resistant to 69 insecticides, while the house fly, German cockroach, and

Colorado potato beetle are each resistant to more than 40 insecticides (Resistant ArthropodDatabase, 2004)

Numerous potential tactics for the management of resistance have been proposed, one

or more of which may be appropriate in a specific pest situation They include (1) increasinguse of non-insecticidal strategies (i.e., an integrated approach to pest control; see Section

751 INSECTS AND HUMANS

4.6); (2) reduction in the amount of insecticide applied (in conjunction with a raising

of the economic injury threshold and more appropriate timing of insecticide application);

(3) increasing the dose applied so that even potentially resistant genotypes are killed; (4) use

of insecticide mixtures (the assumption being that the resistance mechanisms for each

insecticide will be different and will not occur together in individuals); (5) use of rotations

(alternation of the insecticides used) so that resistance to an insecticide decreases during the

intervals between its use; (6) the use of synergists which depress the rate of detoxication;

and (7) development of new forms of insecticides (but see previous paragraphs) (Georghiou,

1983; Roush, in Pimentel, 1991, Vol 2; Denholm and Rowland, 1992)

The second problem associated with insecticide use is one already mentioned in Section

2.3, namely, the non-specificity of action of these chemicals, with the result that beneficial as

well as pest species are destroyed (Indeed, some were developed precisely because of their

“general purpose” nature!) As pest species typically can recover from insecticide application

more rapidly than their natural enemies (because of their greater reproductive potential),

they rebound with even greater force, necessitating additional insecticidal treatment and

increasing costs to the user

The third problem is the potential health hazard, both direct and indirect, of many of the

synthetic insecticides to humans, livestock, and wildlife The World Health Organization

estimated that, on a worldwide basis, about 3 million humans each year are hospitalized

due to exposure to pesticides (herbicides, fungicides and insecticides), and about 220,000

persons die, almost all in developing countries (Jeyaratnam, 1990) It should be noted,

however, that two-thirds of these fatalities are suicides (Palmborg, in Pimentel, 2002)

Indirectly, many millions more, as well as wildlife, receive minute daily doses in their food

and drink or in the air they breathe Indeed, a feature of insecticides originally considered

beneficial, namely, their highly persistent (indestructible) nature in the environment, is now

realized to be a major detriment to their safety For example, DDT is highly stable and only

slowly degraded in the presence of sunlight and oxygen Thus, a single spraying in a house

or barn may remain effective up to a year, and even outdoor applications (on foliage) may be

stable through an entire growing season Unfortunately, this stability is retained following

ingestion or absorption of DDT by living organisms Thus, DDT tends to be stored in

fatty tissue, because of its lipid solubility, and is concentrated as it is transferred from

organism to organism in food webs Recognition of the phenomenon of bioconcentration

(biological magnification) via food webs and observation of harmful effects of insecticides

in the terminal members of food chains (especially predatory birds) led to enormous public

outcry against insecticides As a result, governments have been forced to examine carefully

the balance between the benefits gained and the risks entailed in the use of insecticides,

and where necessary enact legislation to protect human interest One result of this was the

banning in 1972 of DDT use in the United States, in all except a very few situations where

benefits clearly outweighed risks (Whittemore, 1977) Since then, the list of insecticides

whose registration has been fully or partially canceled, suspended pending review, or

modi-fied (e.g., by imposing requirements for protective clothing, changes in application method,

or application by a certified person) in the United States has grown considerably and now

includes virtually all uses of the chlorinated hydrocarbons (Szmedra, in Pimentel, 1991,

Vol 1)

Despite this rather gloomy picture, it must be strongly emphasized that synthetic

insec-ticides have saved and will continue to save millions of human lives and billions of dollars’

worth of food and organic manufactured goods They are still by far the principal method

CHAPTER 24

for control of insect pests, and a good investment for users, with a return of about US$4for each dollar invested, and in their absence losses would increase by a further 10% How-ever, there is a realization among users that insecticides are probably more valuable (i.e.,cheaper and having a longer period of service) when used selectively, in conjunction withother methods such as biological control, rather than in a “blanket” manner as in the past.This is associated with an appreciation that actual extermination of a pest is almost neverachievable, or is even necessary in most situations; that is, a certain amount of pest damagecan be tolerated without suffering economic loss In North America the total amount of in-secticide applied is now declining slightly, reflecting improved application technology thatpermits lower dose rates, improved formulations, more informed application, and a decline

in the number of hectares treated as a result of declining farm economy and greater use ofnon-pesticide control strategies However, on a worldwide basis insecticide use continues

to increase, especially among the less developed nations in Africa and Central and SouthAmerica, where this remains the best method of pest control

The chemicals discussed above mainly operate on the principle of control throughrapid death of (most) members of a pest population More recently, however, great interesthas been shown in other chemicals that, though widely different in nature, are collectivelyknown as insectistatics because they suppress insects’ growth and reproduction (Levinson,1975) They include (1) substances that inhibit chitin synthesis or tanning, rendering aninsect more susceptible to microbial (especially fungal) infection or preventing normal ac-tivity because the muscles do not have a firm structural base; (2) antagonists or analogues ofessential metabolites (e.g., essential amino acids and vitamins) whose effect is to prolonglarval life and/or retard egg production, frequently resulting in death; (3) insect growthregulators (IGRs), substances with juvenile-hormone or ecdysonelike activity; and (4) sexattractants The ability to purify and sequence insect neuropeptides (Chapter 13, Section 3.1)and their corresponding nucleotides has led to speculation about the potential use of thesemolecules or their analogues in pest control Safety may be a concern, however, as a sig-

nificant degree of homology exists between insect and vertebrate peptides (Kelly et al.,

1994)

Some 600 compounds are known to mimic juvenile hormone to various degrees and indifferent species Among the effects of these IGRs are (1) interference with embryogenesis,followed by death, at IGR doses about 1/1000th the value of conventional ovicides; (2) ab-normal development of the integument in postembryonic stages, leading to inability to moltproperly and impaired sensory function (hence inability to locate food, mates, ovipositionsites, etc.); (3) improper metamorphosis of internal organs or external genitalia, causingsterility and/or inability to mate; (4) interference with diapause, so that an insect becomesseasonally maladjusted; and (5) abnormal polymorphism in aphids (Staal, 1975) Becausethese effects take some time to manifest themselves, IGRs are less valuable against rapidlygrowing larval pests However, a number of commercial preparations are now available forinsects that are long-lived pests and/or pests in the adult stage, for example, fenoxycarb(livestock flies), methoprene (fleas, mosquitoes, stored product pests), hydroprene (cock-roaches), and kinoprene (homopteran pests of greenhouses and ornamentals) (Staal, 1987)

As insects presumably do not become resistant to their own hormones, it was suggested thatpests would not develop resistance to these juvenile-hormone analogues Unfortunately,this has not proven to be the case, many examples of cross resistance to juvenile-hormoneanalogues in insects resistant to conventional insecticides being reported in the literature(Sparks and Hammock, 1983; Beckage, in Rechcigl and Rechcigl, 2000)

753 INSECTS AND HUMANS

IGRs that mimic molting hormone have been investigated less intensely, probably due

to their greater structural complexity and relative instability (Dhadialla et al., 1998)

Never-theless, commercial products are available, for example, tebufenozide and halofenozide,

which are used against lepidopteran pests and pests of turf grass and ornamentals,

respec-tively Significantly, tebufenozide is generally non-toxic to non-Lepidoptera, including a

range of predators and parasitoids (Dhadialla et al., 1998).

With the discovery and identification of pheromones (Chapter 13, Section 4.1) and

their mimics (more than 1000 are now known), there were high hopes for the development

of new, effective and environmentally safe methods of pest control As initially envisaged,

the pheromones, especially sex attractants and aggregation pheromones, potentially might

be used in the following pest management situations: (1) for monitoring pest population

density; (2) as lures to attract pests into traps; and (3) for permeating the environment, so

that individuals are unable to locate mates For the first of these possibilities, pheromones

have been an outstanding success and are now an integral component of many pest

man-agement programs, with commercial preparations available for more than 250 species For

some species, especially Coleoptera, the pheromone is used in association with a synergist

kairomone (Chapter 13, Section 4.2); for example, the pheromone of the western pine

bee-tle, Dendroctonus brevicomis, is used together with myrcene, a volatile material produced

by the host tree The second and third possibilities, the “direct” control options, on the other

hand, have met with much less success, principally because of the high costs involved for

the user but also because of reluctance on the part of industry to produce materials with

such specificity of action Nonetheless, commercial mass-trapping systems are available

for 19 species (including 12 Lepidoptera) and mating-disruption formulations for almost

30 species (all Lepidoptera) (Ridgway et al., 1990; Shorey, in Pimentel, 1991, Vol 2; Card´e

and Minks, 1995; Suckling and Karg, in Rechcigl and Rechcigl, 2000) The majority of

these are used against pests of high-value crops, including stone fruits, berries, apples,

grapes, and tomatoes

4.3 Biological Control

Biological control, in the sense used here, may be described as the regulation of pest

populations by natural enemies (parasites, predators, and pathogens) Essentially, it includes

four strategies, depending on the nature of the control agent and the pest: (1) natural (passive)

control in which the agent is an endemic species and the pest is either endemic or introduced;

(2) augmentative control in which populations of an endemic control agent are increased,

either by cultural means in the field or by mass-rearing and release; (3) classical biological

control (perhaps the best known form) where an exotic control agent is imported to control

an introduced, coevolved pest; and (4) neoclassical biological control in which the agent is

an exotic species brought in to control a native pest (Lockwood, 1993) This latter strategy

is, in fact, a specific form of a wider approach known as the “new association” in which

the control agent is an exotic species that has not coevolved with the pest (which may

be native or introduced) (Hokkanen and Pimentel, 1984, 1989; Hokkanen, in Pimentel,

1991, Vol 2) Interwoven among all of these strategies is “conservation biological control”

(Barbosa, 1998) This entails the use of tactics that alter the habitat of the control agent so

as to improve its survival, reproduction, etc., leading to a greater chance of success The

tactics are wide-ranging and include methods that affect the control agent either directly

(e.g., providing it with alternate food sources and nest sites) or indirectly (e.g., adjusting